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In Silico Phylogenetic and Structural Analyses of Plant Endogenous Danger Signaling Molecules Upon Stress

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In Silico Phylogenetic and Structural Analyses of Plant Endogenous Danger Signaling Molecules Upon Stress Hindawi Oxidative Medicine and Cellular Longevity Volume 2019, Article ID 8683054, 14 pages https://doi.org/10.1155/2019/8683054 Research Article In Silico Phylogenetic and Structural Analyses of Plant Endogenous Danger Signaling Molecules upon Stress Athanasia Pavlopoulou ,1 Ezgi Karaca ,1,2 Alma Balestrazzi ,3 and Alexandros G. Georgakilas 4 1Izmir International Biomedicine and Genome Institute, Dokuz Eylül University, 35340 Balcova, Izmir, Turkey 2Izmir Biomedicine and Genome Center, 35340 Balcova, Izmir, Turkey 3Department of Biology and Biotechnology “Lazzaro Spallanzani”, University of Pavia, Via Ferrata 1, 27100 Pavia, Italy 4DNA Damage Laboratory, Department of Physics, School of Applied Mathematical and Physical Sciences, National Technical University of Athens (NTUA), Athens, Greece Correspondence should be addressed to Athanasia Pavlopoulou; [email protected] and Alexandros G. Georgakilas; [email protected] Received 28 December 2018; Revised 3 April 2019; Accepted 23 May 2019; Published 15 July 2019 Academic Editor: Joël R. Drevet Copyright © 2019 Athanasia Pavlopoulou et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The plant innate immune system has two major branches, the pathogen-triggered immunity and the effector-triggered immunity (ETI). The effectors are molecules released by plant attackers to evade host immunity. In addition to the foreign intruders, plants possess endogenous instigators produced in response to general cellular injury termed as damage-associated molecular patterns (DAMPs). In plants, DAMPs or alarmins are released by damaged, stressed, or dying cells following abiotic stress such as radiation, oxidative and drought stresses. In turn, a cascade of downstream signaling events is initiated leading to the upregulation of defense or response-related genes. In the present study, we have investigated more thoroughly the conservation status of the molecular mechanisms implicated in the danger signaling primarily in plants. Towards this direction, we have performed in silico phylogenetic and structural analyses of the associated biomolecules in taxonomically diverse plant species. On the basis of our results, the defense mechanisms appear to be largely conserved within the plant kingdom. Of note, the sequence and/or function of several components of these mechanisms was found to be conserved in animals, as well. At the same time, the molecules involved in plant defense were found to form a dense protein-protein interaction (PPi) network, suggesting a crosstalk between the various defense mechanisms to a variety of stresses, like oxidative stress. 1. Introduction converging theory has emerged that points towards the concept of host perception of “danger” independently of its Plants lack a global immune surveillance system, but they origin [2, 3]. have acquired through evolution a highly effective innate DAMPs as death-, danger-, or damage-associated molec- immune response. There are currently three major types ular patterns are of biological origin and are considered the of elicitors of immune response in plants: (a) the “nonself” major immunogenic mediators released passively by dam- foreign molecule microbial/pathogen-associated molecular aged, stressed, or dying cells, including tumor cells targeted patterns (MAMPs/PAMPs) recognized by surface-localized by oxidative injury, radiation, or chemotherapy [4]. Endoge- pattern recognition receptors (PRRs), (b) signals produced nous or self signals are of two kinds, the primary DAMPS by herbivores, nematodes, or parasitic plants, and (c) their (e.g., cell wall fragments) and the secondary signals produced effectors released by the attackers in order to counteract in response to danger, like processed protein fragments, host defense [1]. Based on the principle on the wide variety such as phytocytokines, similar to animal cytokines. A third of all these patterns inducing immune response, a unifying class that has evolved lately and is not well-defined includes 2 Oxidative Medicine and Cellular Longevity the abiotic danger signals, like nanomaterials [5]. DAMPs genes and the interactions of this network to inflammatory are host cell-derived, as opposed to exogenously derived and immune response networks. DAMPs are regarded as (nonself) MAMPs and PAMPs [6]. In a seminal study on this the link between these networks. Therefore, the analytical field by Matzinger [7], it was suggested that the immune sys- description of the molecular mechanisms and regulatory tem does not actually distinguish between self and nonself pathways that orchestrate plant responses to abiotic stresses but rather detects “danger” through a series of positive and and, particularly, oxidative stress, cell death, and DDR is cru- negative signals derived from damaged or stressed tissues cial for the application of this knowledge to more compli- mediated by DAMPs [7]. In plants, DAMPs, similar to ani- cated organisms. mals, are perceived by pattern recognition receptors (PRRs), Plants’ immune response against intruders is regulated such as plasma membrane-localized receptors, thereby lead- mainly by two antagonistic defense signaling pathways: (i) ing to a cascade of events including cytoplasmic Ca2+ eleva- the salicylic acid- (SA-) mediated signal transduction path- tion, depolarization of the cell membrane, production of way elicited by biotrophic and hemiobiotrophic pathogens reactive oxygen species (ROS), the transient phosphorylation and (ii) the octadecanoid signaling pathway with the key hor- of mitogen-activated protein kinases (MAPKs), and the tran- mone jasmonic acid (JA) induced by heterotrophic patho- scriptional upregulation of defense or response-related genes gens and herbivores [1]. Of note, the oxidized lipids that [6, 8, 9]. In humans, oxidative stress, through the production participate in octadecanoid signaling are the plant functional of ROS, activates components of the MAPK-mediated sig- equivalents of the mammalian oxidized phospholipids [26]. naling pathway including ERK, JNK, and p38 MAPKs; this To date, there is still a knowledge gap concerning the evo- can have both prosurvival and proapoptotic effects [10]. lutionary origin of the different DAMP-dependent signaling Although in yeast and mammals the main mechanisms trig- cascades identified in the plant kingdom and the way this gering MAPK signaling activation under stress conditions valuable knowledge can be projected to more complex organ- have been studied extensively, in plants they remain largely isms, especially animal cells. We believe that an evolutionary unexplored [11]. perspective could provide useful insights into the origin of In plant cells, there is emerging evidence of the connec- DAMP-mediated mechanisms and their role across the dif- tion between DAMPs and the DNA damage response ferent levels of biological organization and complexity. In (DDR), as nucleic acid recognition represents a fundamental this study, we have made an effort to assess the conservation step in host defense. Plants have been documented to per- of the defense mechanisms by conducting phylogenetic and ceive both extracellular DNA and RNA [12–14]. Toll-like structural analyses of the molecules implicated in different receptors (TLRs) play a central role in the preferential recog- stages of danger signaling in 11 vascular plant species that nition and binding of extracellular DNA in animals [15–19]. represent diverse taxonomic divisions: Arabidopsis thaliana Despite the fact that TLR homologs have not been identified (thale cress), Zea mays, Oryza sativa (rice), Hordeum vulgare in plants, extracellular self-DNA (sDNA) was shown to act as (barley), Medicago truncatula (barrel medic), Nicotiana taba- a DAMP in plants. It has been reported that sDNA can trig- cum (tobacco), Populus trichocarpa (cottonwood), Solanum ger ROS- and MAPK-dependent signaling cascades [20], lycopersicum (tomato), Prunus persica (peach), Vitis vinifera alter the CpG DNA methylation status (hypomethylation), (wine grape), and Pisum sativum (pea). and elicit defense-related responses [21]. Moreover, DNA damage and alteration of the primary chromatin structure 2. Methods were shown to induce the expression of defense-related genes [22, 23]. Elucidation of the plant-specific receptors that recog- 2.1. Sequence Dataset and Homology Searching. The biblio- nize extracellular sDNA as DAMPs could advance our knowl- graphic database PubMed/MEDLINE (https://www.ncbi edge on sDNA-dependent danger signaling in plant cells. .nlm.nih.gov/pubmed) was thoroughly searched using rele- Plants have evolved mechanisms of innate immunity vant keywords such as “damage-associated molecular pat- against detrimental pathogenic microorganisms and herbiv- terns”, “danger signals”, “alarmins”, “danger-associated orous animals. As mentioned above, DAMPs or alarmins, molecular patterns”, “DAMPs”, “endogenous danger signal- i.e., biomolecules released by stressed cells, share similarities ing”, “plants”, and “viridiplantae”. The names and/or acces- between plants and animals in different aspects. For example, sion numbers of the characterized proteins reported in the the recently discovered Arabidopsis HMGB3 is the counter- articles were used to retrieve their corresponding sequences part of the pivotal animal DAMP HMGB1 [6]. Recent studies from the publicly accessible sequence databases UniProtKB highlight
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